Invariant odor recognition with ON–OFF neural ensembles

Invariant stimulus recognition is a challenging pattern-recognition problem that must be dealt with by all sensory systems. Since neural responses evoked by a stimulus are perturbed in a multitude of ways, how can this computational capability be achieved? We examine this issue in the locust olfactory system. We find that locusts trained in an appetitive-conditioning assay robustly recognize the trained odorant independent of variations in stimulus durations, dynamics, or history, or changes in background and ambient conditions. However, individual- and population-level neural responses vary unpredictably with many of these variations. Our results indicate that linear statistical decoding schemes, which assign positive weights to ON neurons and negative weights to OFF neurons, resolve this apparent confound between neural variability and behavioral stability. Furthermore, simplification of the decoder using only ternary weights ({+1, 0, −1}) (i.e., an “ON-minus-OFF” approach) does not compromise performance, thereby striking a fine balance between simplicity and robustness.

Patterns of parent and offspring gene expression reflect canalization, not plasticity, in response to environmental stress

Parenting buffers offspring from hostile environments, but it is not clear how or if the genes that underlie parenting change their expression under environmental stress. We recently demonstrated that for the subsocial carrion beetle, Nicrophorus orbicollis, temperature during parenting does not affect parenting phenotypes. Here, we ask if transcriptional changes associated with parenting are likewise robust to environmental stress. The absence of a transcriptional response for parenting under stress would suggest that the genetic programs for parenting and being parented are canalized. Conversely, a robust transcriptional response would suggest that plasticity of underlying gene expression is critical for maintaining behavioral stability, and that these mechanisms provide a potential target for selection in the face of environmental change. We test these alternatives by characterizing gene expression of parents and offspring with and without parent-offspring interactions under a benign and a stressful temperature. We found that parent-offspring interactions elicit distinct transcriptional responses of parents and larvae irrespective of temperature. We further detected robust changes of gene expression in beetles breeding at 24 degrees C compared to 20 degrees C irrespective of family interaction. However, no strong interaction between parent-offspring interaction and temperature was detected for either parents or larvae. We therefore conclude that canalization, not plasticity of gene expression, most likely explains the absence of behavioral plasticity under thermal stress. This result suggests that species may not have the genetic variation needed to respond to all environmental change, especially for complex phenotypes.

Lifetime stability of social traits in bottlenose dolphins

Behavioral phenotypic traits or “animal personalities” drive critical evolutionary processes such as fitness, disease and information spread. Yet the stability of behavioral traits, essential by definition, has rarely been measured over developmentally significant periods of time, limiting our understanding of how behavioral stability interacts with ontogeny. Based on 32 years of social behavioral data for 179 wild bottlenose dolphins, we show that social traits (associate number, time alone and in large groups) are stable from infancy to late adulthood. Multivariate analysis revealed strong relationships between these stable metrics within individuals, suggesting a complex behavioral syndrome comparable to human extraversion. Maternal effects (particularly vertical social learning) and sex-specific reproductive strategies are likely proximate and ultimate drivers for these patterns. We provide rare empirical evidence to demonstrate the persistence of social behavioral traits over decades in a non-human animal.

Behavioral consistency in the digital age

Efforts to infer personality from digital footprints have focused on behavioral stability at the trait level without considering situational dependency. We repeat Shoda, Mischel, and Wright’s (1994) classic study of intraindividual consistency with data on 28,692 days of smartphone usage by 780 people. Using per app measures of ‘pickup’ frequency and usage duration, we found that profiles of daily smartphone usage were significantly more consistent when taken from the same user than from different users (d > 1.46). Random forest models trained on 6 days of behavior identified each of the 780 users in test data with 35.8% / 38.5% (pickup / duration) accuracy. This increased to 73.5% / 75.3% when success was taken as the user appearing in the top 10 predictions (i.e., top 1%). Thus, situation-dependent stability in behavior is present in our digital lives and its uniqueness provides both opportunities and risks to privacy.

Assessing the relationship between routine and schizophrenia symptoms with passively sensed measures of behavioral stability

Increased stability in one’s daily routine is associated with well-being in the general population and often a goal of behavioral interventions for people with serious mental illnesses like schizophrenia. Assessing behavioral stability has been limited in clinical research by the use of retrospective scales, which are susceptible to reporting biases and memory inaccuracies. Mobile passive sensors, which are less susceptible to these sources of error, have emerged as tools to assess behavioral patterns in a range of populations. The present study developed and examined a metric of behavioral stability from data generated by a passive sensing system carried by 61 individuals with schizophrenia for one year. This metric—the Stability Index—appeared orthogonal from existing measures drawn from passive sensors and matched the predictive performance of state-of-the-art features. Specifically, greater stability in social activity (e.g., calls and messages) were associated with lower symptoms, and greater stability in physical activity (e.g., being still) appeared associated with elevated symptoms. This study provides additional support for the predictive value of individualized over population-level data in psychiatric populations. The Stability Index offers also a promising tool for generating insights about the impact of behavioral stability in schizophrenia-spectrum disorders.

Lesion of striatal patches disrupts habitual behaviors and increases behavioral variability

Habits are automated behaviors that are insensitive to changes in behavioral outcomes. Habitual responding is thought to be mediated by striatum, with medial striatum guiding goal-directed action and lateral striatum promoting habits. However, interspersed throughout the striatum are neurochemically differing subcompartments known as patches, which are characterized by distinct molecular profiles relative to the surrounding matrix tissue. These structures have been thoroughly characterized neurochemically and anatomically, but little is known regarding their function. Patches have been shown to be selectively activated during inflexible motor stereotypies elicited by stimulants, suggesting that patches may subserve habitual behaviors. To explore this possibility, we utilized transgenic mice (Sepw1 NP67) expressing Cre recombinase in striatal patches to target these neurons for selective ablation with a virus driving Cre-dependent expression of caspase 3. Mice were then trained to press a lever for sucrose rewards on a variable interval schedule to elicit habitual responding. Mice were not impaired on the acquisition of this task, but lesioning striatal patches disrupted behavioral stability across training and lesioned mice utilized a more goal-directed behavioral strategy during training. Similarly, when mice were forced to omit responses to receive sucrose rewards, habitual responding was impaired in lesioned mice. To rule out effects of lesion on motor behaviors, mice were then tested for impairments in motor learning on a rotarod and locomotion in an open field. We found that patch lesions specifically impaired initial performance on the rotarod without modifying locomotor behaviors in open field. This work indicates that patches promote behavioral stability and habitual responding, adding to a growing literature implicating striatal patches in stimulus-response behaviors.